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Gałęcki, R.; Bakuła, T.; Gołaszewski, J. Role of  Insects in Spread of  Foodborne Pathogens. Encyclopedia. Available online: https://encyclopedia.pub/entry/41365 (accessed on 16 April 2024).
Gałęcki R, Bakuła T, Gołaszewski J. Role of  Insects in Spread of  Foodborne Pathogens. Encyclopedia. Available at: https://encyclopedia.pub/entry/41365. Accessed April 16, 2024.
Gałęcki, Remigiusz, Tadeusz Bakuła, Janusz Gołaszewski. "Role of  Insects in Spread of  Foodborne Pathogens" Encyclopedia, https://encyclopedia.pub/entry/41365 (accessed April 16, 2024).
Gałęcki, R., Bakuła, T., & Gołaszewski, J. (2023, February 17). Role of  Insects in Spread of  Foodborne Pathogens. In Encyclopedia. https://encyclopedia.pub/entry/41365
Gałęcki, Remigiusz, et al. "Role of  Insects in Spread of  Foodborne Pathogens." Encyclopedia. Web. 17 February, 2023.
Role of  Insects in Spread of  Foodborne Pathogens
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This entry is adapted from the peer-reviewed paper 10.3390/foods12040770

Insects play a key role in European agroecosystems. Insects provide important ecosystem services and make a significant contribution to the food chain, sustainable agriculture, the farm-to-fork (F2F) strategy, and the European Green Deal. Edible insects are regarded as a sustainable alternative to livestock. 

foodborne pathogens biosecurity food chain

1. Introduction

Insects (class Insecta) are ubiquitous in the world [1], and they come into direct contact with humans [2][3]. Social attitudes toward insects vary. In some countries, insects are regarded as ectoparasites and pests. However, in some cultures and ethnic groups, insects, as a source of protein and other nutrients, have been a part of the human and livestock diet for many centuries [4]. Many insect species are also used in traditional medicine around the world [5]. Insects are used in production of vaccines and protein preparations [6]. In 2004, extracts from Lucilia sericata larvae became the first insect-based treatment for chronic wounds that has been approved for use in the United States [7]. The venom of the Samsum ant (Pseudomyrmex sp.) has numerous medicinal properties. This powerful antioxidant has been shown to reduce inflammation, relieve pain, inhibit tumor growth, protect the liver, and aid hepatitis treatment [8][9]. Insects are also farmed animals [10]. Honey bees (Apis mellifera) have been exploited for honey for many millennia, whereas domestic silk moths (Bombyx mori) and Chinese oak silk moths (Antheraea pernyi) have long been reared for silk. Insects are also in human and animal diets.
Entomophagy, namely the practice of eating insects, continues to attract the interest of researchers, ecologists, and consumers as a potential solution to feeding the world’s growing population in the coming decades [11][12]. In recent years, insects have emerged as one of the most innovative substrates in human and animal nutrition [13][14]. According to many scientists, edible insects are a major milestone in efforts aiming to diversify protein sources and guarantee global food security [15]. Edible insects are most widely consumed in subtropical and tropical regions, but entomophagy is not highly popular in Western culture [11]. Global insect consumption is difficult to estimate, but, according to the literature, around 2000 insect species are consumed in more than 80 countries [16][17]. The most widely consumed insects belong to the orders Coleoptera (31% of global consumption), Diptera (2%), Hemiptera (10%), Hymenoptera (14%), Isoptera (3%), Lepidoptera (18%), Odonata (3%), and Orthoptera (13%) [18]. Around 1500 species of wild and farmed edible insects are eaten in Africa [19]. Nearly 96 tons of edible insects are consumed in the Democratic Republic of Congo each year, and, in Kinshasa alone, an average family consumes around 300 caterpillars per week [20]. Latin America is the second largest market of edible insects, and entomophagy is most popular in Brazil, Ecuador, Colombia, Mexico, Peru, and Venezuela [21]. The Asian insect market is highly innovative [22]. In Asia, insects are not only popular substrates in food and feed production but are also used in the pharmaceutical industry [22]. Until recently, edible insects had not been regarded as a major food source in Europe. A breakthrough came on 20 December 2017, when a list of novel foods, including insects, was introduced by Commission Implementing Regulation (EU) 2017/2470 [23].
All arguments in favor and against entomophagy should be considered to promote introduction of long-term sustainable solutions on the European food market. Safety of edible insects should also be thoroughly analyzed before these products are authorized for human, companion animal, and livestock consumption. Numerous guidelines have been developed to ensure that edible insects are reared under safe conditions and can be safely used in food and feed production [24][25][26]. Despite the fact that most species of edible insects are harvested without proper biosecurity from the natural environment [27], farmed insects have to meet additional food safety standards and guidelines, including control of foodborne pathogens [28][29][30]. For this reason, microbiological safety of edible insects has to be thoroughly researched before they are approved for mass production. The optimal parameters for insect rearing, processing, and storage have already been described in the relevant regulations, but many edible insect species have not been tested for microbiological safety. Edible insects can be a source of biological hazards, including bacteria that cause foodborne diseases, and insect-based foods can become contaminated in all stages of production, delivery, and consumption. Other biological risks associated with insect farming, such as use of organic side-streams and food wastes in insect nutrition, are often disregarded.

2. The Role of Insects in Spread of Pathogenic Microorganisms and Foodborne Pathogens

Edible insects are regarded as a safe dietary alternative in livestock production [31][32][33]. However, microbiological safety of insect-based foods intended for human consumption is still under debate [29][34]. EFSA outputs on safety evaluation of such products have confirmed safety of edible insect consumption under certain conditions of use [35]. Insect farming can contribute to decreasing prevalence and spread of selected contagious diseases, including foodborne diseases, by eliminating pathogen carriers/reservoirs from the food chain. Due to species specificity and the specific physiology of insects, most entomopathogens do not play a role in epidemiology of zoonoses and do not pose a threat to humans [36]. Arthropods’ ability to transmit foodborne pathogens and vector-borne diseases has been widely researched in the context of food production and the One Health approach [37][38][39]. Edible insects are highly unlikely to act as disease vectors [36][40]. Industrially farmed insects are fed agri-food by-products and plant-based products; therefore, the risk of transmission of zoonotic pathogens is low. Entomopathogens cannot cross the species barrier and cause disease in mammals, which is why edible insects are safe to use in food and feed [36]. It is worth noting that, in some cultures, insects infected with pathogens are regarded as a culinary delicacy or as medicinal products [41][42].
There is no evidence to suggest that edible insects harboring bacterial and viral entomopathogens pose a threat to vertebrates [43][44][45]. However, similar to other foods of animal origin, insect-based foods can raise safety concerns because problems can arise after death of insects and during their processing [46]. Companies that rear and process insects must implement strict sanitary rules to ensure microbiological safety of the end product [10][47][48]. Dedicated processing operations are put into place to eliminate any foodborne pathogens. However, the substrate and end product can become infected during processing. To minimize risk, insect farms should abide by the same biosecurity standards that are applied in the conventional food sector [10][24]. Work surfaces should be disinfected, farm workers should maintain good personal hygiene, farm premises should be regularly cleaned, and safe food preparation and delivery practices should be observed [49]. In farms that have not implemented biosecurity measures, insects and insect-based foods can become contaminated with pathogenic microorganisms transmitted by personnel and pests [50][51]. Therefore, legal regulations, in particular veterinary supervision procedures, should be introduced to guarantee safety of insects as a novel food [52]. Similar to other food products, edible insects are sensitive to deviations from approved production or distribution standards [53][54]. The end product can become contaminated when the required parameters are not observed during acquisition of raw materials, processing (such as drying), transport, storage, and distribution. The associated risks are presented in Table 1. Edible insects as final products should be regularly monitored for presence foodborne pathogens to ensure their safe implementation in the farm-to-fork (F2F) strategy and the European food chain.
Table 1. Possible routes of contamination of edible insects and insect-based foods.
Stages of
Contamination		 Risks Treatment Reference
Substrate
  • (Crickets) Minimal impact of external microbiota.
  • (Crickets) Bacterial endospore counts in crickets fed a standard + farm weed (S + W) diet were significantly lower and thus promising and could reduce risks associated with ready-to-eat insects.
  • Risk of contamination with Salmonella spp. and Campylobacter spp. increases if materials such as used paper egg cartons are utilized in insect rearing. This risk is higher if cartons had been in contact with poultry feces.
   [55][56][57]
Rearing
  • (Crickets) Aspergillus flavus strains with low mycotoxigenic potential were identified in reared crickets, which could point to presence of mycotoxins in edible crickets.
   [55]
Harvest
  • (Crickets) Starvation is not an effective method for reducing microbial loads in edible crickets.
 Gut emptying by starvation prior to killing could reduce the microbial load in the insect gut, but it could also decrease fat and energy content and profitability of production. [58]
Processing
  • (Crickets) High microbial loads of TAC and Enterobacteriaceae were detected in edible crickets, indicating a high risk of rapid spoilage.
  • (Crickets) Sporulating bacteria are a part of the cricket microbiome
  • Food safety risks associated with viruses are very low.
  • Vibrio spp., Streptococcus spp., Staphylococcus spp., Clostridium spp., and Bacillus spp. were identified in several studies on the microbiota of processed edible insects sold online.
 Thermal treatments, novel processing methods (i.e., high-pressure processing), and additional post-processing treatments (acidification, addition of food preservatives, modified atmosphere packaging, etc.) should be applied to extend crickets’ shelf-life. [55][59][60]
Transport   https://ipiff.org/wp-content/uploads/2019/12/IPIFF-Guide-on-Good-Hygiene-Practices.pdf (accessed on: 13.November.2022)  
Preparation
  • Dried mopane worms, termites, and stink bugs sold at the Thohoyandou market were characterized by low contamination with coliforms, Escherichia coli, Staphylococcus aureus, Salmonella spp., TPC, yeasts, and molds.
   [61]
Storage
  • (T. molitor, Alphitobius diaperinus, Gryllus assimilis, Lo. Migratoria) microbiological characteristics in different storage periods—safe for human consumption.
 Insects intended for long-term storage should be killed in boiling water, dried at 103 °C for 12 h, and hermetically packed. [62]
Consumption
  • The nutritional value and the microbiological and toxicological profiles of insects are influenced by composition of organic side streams.
  • The microbial risks associated with edible insects can be substantially reduced by observing good hygienic practices in rearing, handling, harvesting, processing, storage, and transport of insects and insect-based products.
  • Several spoilage-causing microbes that can alter food quality, including Lysinibacillus sp. and Bacillus subtilis, have been detected in edible insects.
  • Yeasts, including Tetrapisispora spp., Candida spp., Pichia spp., and Debaryomyces spp., and molds, including Aspergillus spp., Alternaria spp., Cladosporium spp., Fusarium spp., Penicillium spp., Phycomycetes spp., and Wallemia spp., are associated with the microbiota found on the body surface or in the gut of edible insects and may be harmful.
  • 38 samples of deep-fried and spiced Ach. Domesticus, Lo. Migratoria, and Omphisa fuscidentalis tested negative for Salmonella spp., Listeria monocytogenes, E. coli, and S aureus, but dried and powdered insects, as well as pollen, contained Bacillus cereus, coliforms, Serratia liquefaciens, Listeria ivanovii, Mucor spp., Aspergillus spp., Penicillium spp., and Cryptococcus neoformans.
   [18][28][59][63]
R&D
  • (Crickets) Further efforts are needed to identify food-borne pathogens in edible crickets and define possible bacterial quality reference values.
   [55]
Consumption of unprocessed insects may represent a significant risk factor. Insects can act as mechanical or biological vectors of pathogens [37], particularly critical priority pathogens in the food processing industry, including Bacillus spp., Clostridium spp., E. coli, L. monocytogenes, Salmonella spp., and Staphylococcus spp. [64][65][66][67]. Bacteriological hazards have been most widely investigated, but insects can also act as intermediate hosts or mechanical vectors for parasites in the natural environment [38]. Therefore, effective processing operations should be implemented and sanitary guidelines should be observed to minimize risk of contamination with foodborne pathogens [51].
Allergenicity of edible insects is yet another important safety concern. Similar to other food products, edible insects could pose certain risks to consumers with allergies. To date, 239 arthropod allergens have been identified by the Allergen Nomenclature Sub-committee of the World Health Organization (WHO) [68]. Edible insects may also cause cross-reactivity in people allergic to seafood. The following allergens are most frequently identified in edible insects: fructose-bisphosphate aldolase, phospholipase A, hyaluronidase, arginine kinase, myosin light chain, tropomyosin, α-tubulin, and β-tubulin [69]. A total of 116 allergic reactions to edible insects, mostly grasshoppers, locusts, and lentil weevils, have been identified in 2018 [68]. Insect allergens induce non-specific symptoms, such as anaphylaxis, allergic asthma, hypotension, gastrointestinal symptoms, loss of consciousness, urticaria, erythema, pruritus, and tachycardia. Employees of insect farms and insect processing plants can also develop allergic reactions [70][71]. Allergies also pose a threat to companion animals. Insects can also harbor foreign allergens [69][72], including mites and their metabolites. Direct contact with new proteins or symbiotic organisms can trigger heightened immune response. Presence of gluten in digestive tracts of insects fed grain [73] can pose a threat to people who suffer from celiac disease. Allergizing potential of edible insects should be monitored to eliminate these risks. Potential allergens in insect-based foods should be clearly listed on the product label.
Prions pose a significant biological hazard. Prions are one of the key hazards that have been identified by the European Food Safety Authority (EFSA) in the risk profile of edible insects [34][43]. Insect-specific prion diseases have not been identified because insects lack the gene encoding the prion protein PrP [34][74]. However, insects may act as vectors for prions from contaminated substrates derived from ruminants, which could pose a risk for humans, companion animals, and livestock [34][43].
At present, there is no scientific evidence to suggest that insects pose a viral risk to consumers [43][44][75][76]. Entomoviruses are not pathogenic to humans. Insects are commonly infected with viruses of the family Baculoviridae, which are not dangerous for humans or animals [36][77]. Humans do not harbor insect-specific viruses, and there is negligible risk that new mammalian-specific virus strains will evolve through recombination and reassortment and lead to host switching, as was the case with Swine flu [36]. Edible insects are unlikely to transmit foodborne viruses, such as Hepadnaviridae (hepatitis A and E), Reoviridae (reoviruses), and Caliciviridae (noroviruses) [50]. However, viruses could be transmitted to insects through feed or through contact with farm personnel. Viruses of the family Rhabdoviridae, which cause vesicular stomatitis, have been reported in edible insects [54]. Risk of SARS-CoV-2 transmission by edible insects is very low [36][76][78]. According to Doi et al. [36], risk of infection with SARS-CoV-2 as a foodborne pathogen is negligent in people who consume edible insects [36]. It should be noted that viruses causing foodborne diseases do not replicate in arthropods [44][75], but edible insects could become contaminated during processing and distribution.
Bacteria are presently regarded as the greatest safety hazard in production of edible insects [47]. Due to physiological, environmental, and behavioral differences, every species of edible insects intended for food and feed production harbors different bacteria [66][79]. According to the literature, the microbiome of edible insects poses a negligent risk to consumer safety [80][81]. Several bacteria that can act as opportunist pathogens in humans have been identified in edible insects, but these pathogens are specific to mammals [66]. The risks associated with bacterial symbionts in insects or their potential effects on vertebrates have not been evaluated to date. Insects can act as vectors and carriers of microorganisms that are harmful to humans, particularly when biosecurity and hygiene standards are not observed in insect farms. Insects can carry bacteria that are dangerous to humans, companion animals, and livestock and can act as vectors of foodborne pathogens [82]. Insect microbiota typically include the following bacterial families and genera: Enterobacteriaceae (Proteus spp., Escherichia spp.), Pseudomonas spp., Staphylococcus spp., Streptococcus spp., Bacillus spp., Micrococcus spp., Lactobacillus spp., and Acinetobacter spp. [83]. Some species of the above families and genera are potentially pathogenic to humans, whereas others are commonly encountered in healthy subjects. Unprocessed insects and insect-based foods can harbor Campylobacter spp., verotoxic E. coli, Salmonella spp., and L. monocytogenes if microbial inactivation techniques are not applied in production plants. Therefore, insects and insect-based foods should always be screened for these pathogens. Prevalence of some of these pathogens is lower in insects than in other animal protein sources. For example, Campylobacter spp. is not replicated in the digestive tract of insects [84][85][86]. Similar risks can be encountered during insect processing. Several bacterial species identified in edible insects can shorten the shelf-life of the final product. Presence of spore-forming bacteria in the end product poses one of the greatest bacteriological hazards [87]. Common sanitation practices, such as drying, boiling, or deep frying, may not be sufficient to eliminate these pathogens.
Entomopathogenic fungi are yet another group of potentially hazardous organisms. There is no scientific evidence to suggest that entomopathogenic fungi pose a risk to vertebrates. In some cultures, these fungi (such as Ophiocordyceps sinensis) have long been used in traditional medicine [41]. Mycosporidia could also pose a health threat to consumers [88], but their toxicity has not been analyzed to date. According to the literature, microsporidia Trachipleistophora spp. that probably originated from insects can infect vertebrates [89][90]. Due to specific insect rearing conditions and administered feeds, the end product can become contaminated with mycotoxins [91][92]. High concentrations of mycotoxins, such as deoxynivalenol, can lead to gastrointestinal dysfunction in mammals. Molds can also develop in insect-based products that have been stored and distributed in sub-optimal conditions. However, presence of molds in insect-based products has not been reported in the literature. Risks associated with fungi and mycotoxins in insect-derived foods are often disregarded, and further research is needed to guarantee safety of the end product.
Edible insects can potentially transmit parasitic diseases [38][93]. It appears that entomopathogenic parasites are unable to complete their full life cycle in humans or livestock due to biological specificity of the host. Entomopathogenic parasites cannot be transmitted between vertebrates either. However, there is evidence to suggest that some insect-specific parasites can cause digestive problems (such as horsehair worms, Gordius spp.) [94] or allergies (Lophomonas blattarum) [95]. Insects can also act as intermediate hosts for foodborne pathogens, including tapeworms (Hymenolepis spp.), lancet liver flukes (Dicrocoelium dendriticum), and nematodes (Spirocerca lupi) [93][96][97][98]. Insects can also act as mechanical vectors for different developmental stages of vertebrate parasites in different stages of their life cycle [38][99]. Insects can transmit parasites that colonize body surfaces (hairs, chitin exoskeletons) and digestive tracts. Mechanical transmission of parasites is a serious concern during insect farming. Research has demonstrated that insects can transmit protozoa [93][100][101]. It should also be noted that insects themselves can act as etiological factors of disease. Beetles of the family Tenebrionidae, such as yellow mealworms (T. molitor) and lesser mealworms (A. diaperinus), can cause canthariasis [102][103][104]. Insect farms can also be colonized by mites [105]. Table 2 provides a summary of potential biological hazards.
Table 2. Biological hazards associated with different species of edible insects.
Type of Hazard Infectious Agent Sensitive Species Predisposing Factors References
Prion vectors Proteinaceous infectious particles All species fed contaminated substrates of animal origin
  • inadequate rearing practices
  • failure to observe legal regulations
  • contaminated feed and litter
  • handling operations
  • absence of biosecurity measures
  • sanitation requirements are not observed by farm personnel
 [34][74]
Viruses Caliciviridae
Hepadnaviridae
Vesicular stomatitis virus (VSV)		 Migratory locust (Lo. migratoria),
black soldier fly (H. illucens)
Insects harvested from the natural environment
  • insects are reared with other animals
  • absence of biosecurity measures
  • sanitation requirements are not observed
 [50][54]
Bacteria Aeromonas hydrophila, B. cereus, Clostridium difficile, Clostridium perfringens, Clostridium septicum, Clostridium sporogenes, E. coli, Enterococcus faecium, Enterococcus faecalis, Listeria spp., Salmonella spp., S. aureus. Migratory locust (Lo. migratoria)
Yellow mealworm (T. molitor)
Lesser mealworm (A. diaperinus)
House cricket (Ach. domesticus)
Domestic silk moth (B. mori)
Insects harvested from the natural environment
  • handling operations
  • deviations from production standards
  • rearing conditions
  • inadequate rearing practices
  • contamination of feed and litter
 [64][65][66][67][83]
Fungi and mycotoxins Aspergillus fumigatus, Aspergillus sclerotiorum, Cladosporium spp. Penicillium spp., Fusarium spp., Phycomycetes spp.
Microsporidia		 Migratory locust (Lo. migratoria)
Black soldier fly (H. illucens)
Yellow mealworm (T. molitor)
  • high humidity
  • contamination of feed and litter
  • high water activity in the end product
  • inadequate storage conditions
 [28][48][91][106]
Parasites Protozoa (Balantidium spp., Cryptosporidium spp., Entamoeba spp.)
Trematoda (Dicrocoelium spp., Lecithodendriidae)
Cestoda (Hymenolepis spp., Raillietina spp.)
Nematoda (Gordius spp., Spirocerca spp.)		 Yellow mealworm (T. molitor)
Lesser mealworm (A. diaperinus)
House cricket (Ach domesticus)
Insects harvested from the natural environment
  • insects as vectors of parasitic infections
  • insects as intermediate hosts
  • insects harvested in the natural environment
  • absence of biosecurity measures
  • dirty and contaminated feed (such as unwashed vegetables)
  • presence of pests
  • farm/processing personnel do not observe sanitation requirements
  • insects are reared with other animals
 [4][93][94][95][96][97][98][99][100][101]
Mites Acarus spp., Dermatophagoides spp., Goheria spp. Tyrophagus spp. Mealworm (T molitor)
Lesser mealworm (A. diaperinus)
Black soldier fly (H. illucens)
House cricket (Ach. domesticus)
  • feed substrates are contaminated with mites in different stages of the life cycle
  • biosecurity measures are not observed
  • sanitation requirements are not observed
  • high humidity
  • residual feed is not removed from farm premises
 [105]

This research was supported by a research project Lider XII entitled “Development of an insect protein food for companion animals with diet-dependent enteropathies”, financed by the National Center for Research and Development (NCBiR) (LIDER/5/0029/L12/20/NCBR/2021).

References

  1. Scudder, G.G. The importance of insects. Insect Biodivers. Sci. Soc. 2017, 1, 9–43.
  2. Busvine, J.R. Insects and hygiene. In Insects and Hygiene; Springer: Berlin/Heidelberg, Germany, 1980; pp. 1–20.
  3. Meyer-Rochow, V.B. Can Insects Help to Ease Problem of World Food Shortage. Search 1975, 6, 261–262.
  4. Govorushko, S. Human–Insect Interactions; CRC Press: Boca Raton, FL, USA, 2018.
  5. Dossey, A.T. Insects and their chemical weaponry: New potential for drug discovery. Nat. Prod. Rep. 2010, 27, 1737–1757.
  6. Qian, L.; Deng, P.; Chen, F.; Cao, Y.; Sun, H.; Liao, H. The exploration and utilization of functional substances in edible insects: A review. Food Prod. Process. Nutr. 2022, 4, 11.
  7. Heuer, H.; Heuer, L.; Saalfrank, V. Living Medication: Overview and Classification into Pharmaceutical Law. In Nature Helps....; Springer: Berlin/Heidelberg, Germany, 2011; pp. 349–367.
  8. Altman, R.D.; Schultz, D.R.; Collins-Yudiskas, B.; Aldrich, J.; Arnold, P.I.; Arnold, P.I.; Brown, H.E. The effects of a partially purified fraction of an ant venom in rheumatoid arthritis. Arthritis Rheum. Off. J. Am. Coll. Rheumatol. 1984, 27, 277–284.
  9. Agarwal, S.; Sharma, G.; Verma, K.; Latha, N.; Mathur, V. Pharmacological potential of ants and their symbionts—A review. Entomol. Exp. Et Appl. 2022, 170, 1032–1048.
  10. Żuk-Gołaszewska, K.; Gałęcki, R.; Obremski, K.; Smetana, S.; Figiel, S.; Gołaszewski, J. Edible Insect Farming in the Context of the EU Regulations and Marketing—An Overview. Insects 2022, 13, 446.
  11. Van Huis, A. Potential of insects as food and feed in assuring food security. Annu. Rev. Entomol. 2013, 58, 563–583.
  12. Verbeke, W. Profiling consumers who are ready to adopt insects as a meat substitute in a Western society. Food Qual. Prefer. 2015, 39, 147–155.
  13. Rumpold, B.A.; Schlüter, O.K. Nutritional composition and safety aspects of edible insects. Mol. Nutr. Food Res. 2013, 57, 802–823.
  14. Patel, S.; Suleria, H.A.R.; Rauf, A. Edible insects as innovative foods: Nutritional and functional assessments. Trends Food Sci. Technol. 2019, 86, 352–359.
  15. Kinyuru, J.; Ndung’u, N. Promoting edible insects in Kenya: Historical, present and future perspectives towards establishment of a sustainable value chain. J. Insects Food Feed. 2020, 6, 51–58.
  16. Van Huis, A.; Halloran, A.; Van Itterbeeck, J.; Klunder, H.; Vantomme, P. How many people on our planet eat insects: 2 billion? J. Insects Food Feed. 2022, 8, 1–4.
  17. Jongema, Y. List of Edible Insects of the World; Laboratory of Entomology, Wageningen University: Wageningen, The Netherlands, 2017.
  18. FAO. Looking at Edible Insects from a Food Safety Perspective. Challenges and Opportunities for the Sector; FAO: Rome, Italy, 2021.
  19. Ebenebe, C.I.; Ibitoye, O.S.; Amobi, I.M.; Okpoko, V.O. African edible insect consumption market. In African Edible Insects as Alternative Source of Food, Oil, Protein and Bioactive Components; Springer: Berlin/Heidelberg, Germany, 2020; pp. 19–51.
  20. Kitsa, K. Contribution des insectes comestibles à l’amélioration de la ration alimentaire au Kasaï-Occidental. Zaïre-Afr. Économie Cult. Vie Soc. 1989, 29, 511–519.
  21. Costa-Neto, E.M. Anthropo-entomophagy in Latin America: An overview of the importance of edible insects to local communities. J. Insects Food Feed. 2015, 1, 17–23.
  22. Han, R.; Shin, J.T.; Kim, J.; Choi, Y.S.; Kim, Y.W. An overview of the South Korean edible insect food industry: Challenges and future pricing/promotion strategies. Entomol. Res. 2017, 47, 141–151.
  23. Commission Implementing Regulation (EU). 2017/2469 of 20 December 2017 Laying Down Administrative and Scientific Requirements for Applications Referred to in Article 10 of Regulation (EU) 2015/2283 of the European Parliament and of the Council on Novel Foods; European Union: Luxemburg, 2017.
  24. IPIFF Guide on Good Hygiene Practices for European Union Producers of Insects as Food and Feed. Available online: https://ipiff.org/wp-content/uploads/2019/12/IPIFF-Guide-on-Good-Hygiene-Practices.pdf (accessed on 6 January 2022).
  25. Lähteenmäki-Uutela, A.; Marimuthu, S.; Meijer, N. Regulations on insects as food and feed: A global comparison. J. Insects Food Feed. 2021, 7, 849–856.
  26. Niassy, S.; Omuse, E.; Roos, N.; Halloran, A.; Eilenberg, J.; Egonyu, J.; Tanga, C.; Meutchieye, F.; Mwangi, R.; Subramanian, S. Safety, regulatory and environmental issues related to breeding and international trade of edible insects in Africa. Rev. Sci. Tech. 2022, 41, 117–131.
  27. Feng, Y.; Chen, X.M.; Zhao, M.; He, Z.; Sun, L.; Wang, C.Y.; Ding, W.F. Edible insects in China: Utilization and prospects. Insect Sci. 2018, 25, 184–198.
  28. Grabowski, N.T.; Klein, G. Microbiology of processed edible insect products–results of a preliminary survey. Int. J. Food Microbiol. 2017, 243, 103–107.
  29. Belluco, S.; Losasso, C.; Maggioletti, M.; Alonzi, C.; Ricci, A.; Paoletti, M.G. Edible insects: A food security solution or a food safety concern? Anim. Front. 2015, 5, 25–30.
  30. Belluco, S.; Losasso, C.; Maggioletti, M.; Alonzi, C.C.; Paoletti, M.G.; Ricci, A. Edible insects in a food safety and nutritional perspective: A critical review. Compr. Rev. Food Sci. Food Saf. 2013, 12, 296–313.
  31. Gahukar, R. Edible insects farming: Efficiency and impact on family livelihood, food security, and environment compared with livestock and crops. In Insects as Sustainable Food Ingredients; Elsevier: Amsterdam, The Netherlands, 2016; pp. 85–111.
  32. Dobermann, D.; Swift, J.; Field, L. Opportunities and hurdles of edible insects for food and feed. Nutr. Bull. 2017, 42, 293–308.
  33. Imathiu, S. Benefits and food safety concerns associated with consumption of edible insects. NFS J. 2020, 18, 1–11.
  34. Belluco, S.; Mantovani, A.; Ricci, A. Edible insects in a food safety perspective. In Edible Insects in Sustainable Food Systems; Springer: Berlin/Heidelberg, Germany, 2018; pp. 109–126.
  35. Precup, G.; Ververis, E.; Azzollini, D.; Rivero-Pino, F.; Zakidou, P.; Germini, A. The Safety Assessment of Insects and Products Thereof as Novel Foods in the European Union. Novel Foods and Edible Insects in the European Union; EU: Brussels, Belgium, 2022; p. 123.
  36. Doi, H.; Gałęcki, R.; Mulia, R.N. The merits of entomophagy in the post COVID-19 world. Trends Food Sci. Technol. 2021, 110, 849–854.
  37. Zurek, L.; Gorham, J.R. Insects as Vectors of Foodborne Pathogens. Wiley Handbook of Science and Technology for Homeland Security; Wiley: Hoboken, NJ, USA, 2008; p. 1.
  38. Graczyk, T.K.; Knight, R.; Tamang, L. Mechanical transmission of human protozoan parasites by insects. Clin. Microbiol. Rev. 2005, 18, 128–132.
  39. Lounibos, L.P. Invasions by insect vectors of human disease. Annu. Rev. Entomol. 2002, 47, 233.
  40. Yates-Doerr, E. The world in a box? Food security, edible insects, and “One World, One Health” collaboration. Soc. Sci. Med. 2015, 129, 106–112.
  41. Cao, L.; Ye, Y.; Han, R. Fruiting body production of the medicinal Chinese caterpillar mushroom, Ophiocordyceps sinensis (Ascomycetes), in artificial medium. Int. J. Med. Mushrooms 2015, 17, 1107–1112.
  42. Evans, J.; Müller, A.; Jensen, A.; Dahle, B.; Flore, R.; Eilenberg, J.; Frøst, M. A descriptive sensory analysis of honeybee drone brood from Denmark and Norway. J. Insects Food Feed. 2016, 2, 277–283.
  43. EFSA Scientific Committee. Scientific opinion on a risk profile related to production and consumption of insects as food and feed. EFSA J. 2015, 13, 4257.
  44. van der Fels-Klerx, H.; Camenzuli, L.; Belluco, S.; Meijer, N.; Ricci, A. Food safety issues related to uses of insects for feeds and foods. Compr. Rev. Food Sci. Food Saf. 2018, 17, 1172–1183.
  45. Dall’Asta, C. Why ‘New’Foods Are Safe and How They Can Be Assessed. Novel Foods and Edible Insects in the European Union; EU: Brussels, Belgium, 2022; p. 81.
  46. Lacey, L.A.; Siegel, J.P. Safety and ecotoxicology of entomopathogenic bacteria. In Entomopathogenic Bacteria: From Laboratory to Field Application; Springer: Berlin/Heidelberg, Germany, 2000; pp. 253–273.
  47. Klunder, H.; Wolkers-Rooijackers, J.; Korpela, J.M.; Nout, M.R. Microbiological aspects of processing and storage of edible insects. Food Control 2012, 26, 628–631.
  48. Mutungi, C.; Irungu, F.; Nduko, J.; Mutua, F.; Affognon, H.; Nakimbugwe, D.; Ekesi, S.; Fiaboe, K. Postharvest processes of edible insects in Africa: A review of processing methods, and the implications for nutrition, safety and new products development. Crit. Rev. Food Sci. Nutr. 2019, 59, 276–298.
  49. Rizou, M.; Galanakis, I.M.; Aldawoud, T.M.; Galanakis, C.M. Safety of foods, food supply chain and environment within the COVID-19 pandemic. Trends Food Sci. Technol. 2020, 102, 293–299.
  50. Bakuła, T.; Gałęcki, R. Strategia Wykorzystania Alternatywnych Źródeł Białka w Żywieniu Zwierząt Oraz Możliwości Rozwoju Jego Produkcji na Terytorium Rzeczpospolitej Polski; ERZET: Olsztyn, Poland, 2021; ISBN 978-83-961897-1-4.
  51. Kwiatek, K.; Bakuła, T.; Sieradzki, Z.; Osiński, Z.; Kowalczyk, E. Wytyczne Dobrej Praktyki Higienicznej w Produkcji Owadów dla Celów Paszowych i Spożywczych; Zakład Higieny Pasz Państwowy Instytut Weterynaryjny—Państwowy Instytut Badawczy: Puławy, Poland, 2021; p. 169. Available online: https://www.gov.pl/web/rolnictwo/wytyczne-dobrej-praktyki-higienicznej-w-produkcji-owadow-dla-celow-paszowych-i-spozywczych (accessed on 12 February 2022).
  52. Belluco, S.; Halloran, A.; Ricci, A. New protein sources and food legislation: The case of edible insects and EU law. Food Secur. 2017, 9, 803–814.
  53. Vandeweyer, D.; Crauwels, S.; Lievens, B.; Van Campenhout, L. Metagenetic analysis of the bacterial communities of edible insects from diverse production cycles at industrial rearing companies. Int. J. Food Microbiol. 2017, 261, 11–18.
  54. Fraqueza, M.J.R.; Patarata, L. Constraints of HACCP application on edible insect for food and feed. Future foods 2017, 89–113. Available online: https://books.google.co.jp/books?hl=pl&lr=&id=SW2PDwAAQBAJ&oi=fnd&pg=PA89&dq=Constraints+of+HACCP+application+on+edible+insect+for+food+and+feed.&ots=zxgVfrH4j8&sig=G6_KoH3yMYyO8Z62vfC2Jhws2nc&redir_esc=y#v=onepage&q=Constraints%20of%20HACCP%20application%20on%20edible%20insect%20for%20food%20and%20feed.&f=false (accessed on 16 February 2022).
  55. Fernandez-Cassi, X.; Söderqvist, K.; Bakeeva, A.; Vaga, M.; Dicksved, J.; Vagsholm, I.; Jansson, A.; Boqvist, S. Microbial communities and food safety aspects of crickets (Acheta domesticus) reared under controlled conditions. J. Insects Food Feed. 2020, 6, 429–440.
  56. Ng’ang’a, J.; Imathiu, S.; Fombong, F.; Borremans, A.; Van Campenhout, L.; Broeck, J.V.; Kinyuru, J. Can farm weeds improve the growth and microbiological quality of crickets (Gryllus bimaculatus)? J. Insects Food Feed. 2020, 6, 199–209.
  57. Walia, K.; Kapoor, A.; Farber, J. Qualitative risk assessment of cricket powder to be used to treat undernutrition in infants and children in Cambodia. Food Control 2018, 92, 169–182.
  58. Inacio, A.C.; Vågsholm, I.; Jansson, A.; Vaga, M.; Boqvist, S.; Fraqueza, M. Impact of starvation on fat content and microbial load in edible crickets (Acheta domesticus). J. Insects Food Feed. 2021, 7, 1143–1147.
  59. Vandeweyer, D.; Lievens, B.; Van Campenhout, L. Identification of bacterial endospores and targeted detection of foodborne viruses in industrially reared insects for food. Nat. Food 2020, 1, 511–516.
  60. Fasolato, L.; Cardazzo, B.; Carraro, L.; Fontana, F.; Novelli, E.; Balzan, S. Edible processed insects from e-commerce: Food safety with a focus on the Bacillus cereus group. Food Microbiol. 2018, 76, 296–303.
  61. Ramashia, S.; Tangulani, T.; Mashau, M.; Nethathe, B. Microbiological quality of different dried insects sold at Thohoyandou open market, South Africa. Food Res. 2020, 4, 2247–2255.
  62. Adámek, M.; Mlček, J.; Adámková, A.; Suchánková, J.; Janalíková, M.; Borkovcová, M.; Bednářová, M. Effect of different storage conditions on the microbiological characteristics of insect. Potravin. Slovak J. Food Sci. 2018, 12, 248–253.
  63. Kooh, P.; Ververis, E.; Tesson, V.; Boué, G.; Federighi, M. Entomophagy and public health: A review of microbiological hazards. Health 2019, 11, 1272–1290.
  64. Borch, E.; Arinder, P. Bacteriological safety issues in red meat and ready-to-eat meat products, as well as control measures. Meat Sci. 2002, 62, 381–390.
  65. Balta, I.; Linton, M.; Pinkerton, L.; Kelly, C.; Stef, L.; Pet, I.; Stef, D.; Criste, A.; Gundogdu, O.; Corcionivoschi, N. The effect of natural antimicrobials against Campylobacter spp. and its similarities to Salmonella spp, Listeria spp., Escherichia coli, Vibrio spp., Clostridium spp. and Staphylococcus spp. Food Control 2021, 121, 107745.
  66. Garofalo, C.; Osimani, A.; Milanović, V.; Taccari, M.; Cardinali, F.; Aquilanti, L.; Riolo, P.; Ruschioni, S.; Isidoro, N.; Clementi, F. The microbiota of marketed processed edible insects as revealed by high-throughput sequencing. Food Microbiol. 2017, 62, 15–22.
  67. Chiang, Y.-C.; Tsen, H.-Y.; Chen, H.-Y.; Chang, Y.-H.; Lin, C.-K.; Chen, C.-Y.; Pai, W.-Y. Multiplex PCR and a chromogenic DNA macroarray for the detection of Listeria monocytogens, Staphylococcus aureus, Streptococcus agalactiae, Enterobacter sakazakii, Escherichia coli O157: H7, Vibrio parahaemolyticus, Salmonella spp. and Pseudomonas fluorescens in milk and meat samples. J. Microbiol. Methods 2012, 88, 110–116.
  68. de Gier, S.; Verhoeckx, K. Insect (food) allergy and allergens. Mol. Immunol. 2018, 100, 82–106.
  69. Ribeiro, J.C.; Cunha, L.M.; Sousa-Pinto, B.; Fonseca, J. Allergic risks of consuming edible insects: A systematic review. Mol. Nutr. Food Res. 2018, 62, 1700030.
  70. Pener, M.P. Allergy to crickets: A review. J. Orthoptera Res. 2016, 25, 91–95.
  71. Pomés, A.; Mueller, G.A.; Randall, T.A.; Chapman, M.D.; Arruda, L.K. New insights into cockroach allergens. Curr. Allergy Asthma Rep. 2017, 17, 1–16.
  72. Pali-Schöll, I.; Meinlschmidt, P.; Larenas-Linnemann, D.; Purschke, B.; Hofstetter, G.; Rodríguez-Monroy, F.A.; Einhorn, L.; Mothes-Luksch, N.; Jensen-Jarolim, E.; Jäger, H. Edible insects: Cross-recognition of IgE from crustacean-and house dust mite allergic patients, and reduction of allergenicity by food processing. World Allergy Organ. J. 2019, 12, 100006.
  73. Mancini, S.; Fratini, F.; Tuccinardi, T.; Degl’Innocenti, C.; Paci, G. Tenebrio molitor reared on different substrates: Is it gluten free? Food Control 2020, 110, 107014.
  74. Van Raamsdonk, L.; Van der Fels-Klerx, H.; De Jong, J. New feed ingredients: The insect opportunity. Food Addit. Contam. Part A 2017, 34, 1384–1397.
  75. Eilenberg, J.; Vlak, J.; Nielsen-LeRoux, C.; Cappellozza, S.; Jensen, A. Diseases in insects produced for food and feed. J. Insects Food Feed. 2015, 1, 87–102.
  76. Dicke, M.; Eilenberg, J.; Salles, J.F.; Jensen, A.; Lecocq, A.; Pijlman, G.; Van Loon, J.; Van Oers, M. Edible insects unlikely to contribute to transmission of coronavirus SARS-CoV-2. J. Insects Food Feed. 2020, 6, 333–339.
  77. Paul, A.; Hasan, A.; Rodes, L.; Sangaralingam, M.; Prakash, S. Bioengineered baculoviruses as new class of therapeutics using micro and nanotechnologies: Principles, prospects and challenges. Adv. Drug Deliv. Rev. 2014, 71, 115–130.
  78. Roundy, C.M.; Hamer, S.A.; Zecca, I.B.; Davila, E.B.; Auckland, L.D.; Tang, W.; Gavranovic, H.; Swiger, S.L.; Tomberlin, J.K.; Fischer, R.S.B.; et al. No Evidence of SARS-CoV-2 Among Flies or Cockroaches in Households Where COVID-19 Positive Cases Resided. J. Med. Entomol. 2022, 59, 1479–1483.
  79. Osimani, A.; Milanović, V.; Garofalo, C.; Cardinali, F.; Roncolini, A.; Sabbatini, R.; De Filippis, F.; Ercolini, D.; Gabucci, C.; Petruzzelli, A. Revealing the microbiota of marketed edible insects through PCR-DGGE, metagenomic sequencing and real-time PCR. Int. J. Food Microbiol. 2018, 276, 54–62.
  80. Boemare, N.; Laumond, C.; Mauleon, H. The entomopathogenic nematode-bacterium complex: Biology, life cycle and vertebrate safety. Biocontrol Sci. Technol. 1996, 6, 333–346.
  81. Kikuchi, Y. Endosymbiotic bacteria in insects: Their diversity and culturability. Microbes Environ. 2009, 24, 195–204.
  82. Grabowski, N.T.; Klein, G. Bacteria encountered in raw insect, spider, scorpion, and centipede taxa including edible species, and their significance from the food hygiene point of view. Trends Food Sci. Technol. 2017, 63, 80–90.
  83. Amadi, E.; Ogbalu, O.; Barimalaa, I.; Pius, M. Microbiology and nutritional composition of an edible larva (Bunaea alcinoe Stoll) of the Niger Delta. J. Food Saf. 2005, 25, 193–197.
  84. Templeton, J.M.; De Jong, A.J.; Blackall, P.; Miflin, J.K. Survival of Campylobacter spp. in darkling beetles (Alphitobius diaperinus) and their larvae in Australia. Appl. Environ. Microbiol. 2006, 72, 7909–7911.
  85. Strother, K.O.; Steelman, C.D.; Gbur, E. Reservoir competence of lesser mealworm (Coleoptera: Tenebrionidae) for Campylobacter jejuni (Campylobacterales: Campylobacteraceae). J. Med. Entomol. 2005, 42, 42–47.
  86. Wales, A.; Carrique-Mas, J.; Rankin, M.; Bell, B.; Thind, B.; Davies, R. Review of the carriage of zoonotic bacteria by arthropods, with special reference to Salmonella in mites, flies and litter beetles. Zoonoses Public Health 2010, 57, 299–314.
  87. Osimani, A.; Aquilanti, L. Spore-forming bacteria in insect-based foods. Curr. Opin. Food Sci. 2021, 37, 112–117.
  88. Stentiford, G.; Becnel, J.; Weiss, L.; Keeling, P.; Didier, E.; Bjornson, S.; Freeman, M.; Brown, M.; Roesel, K.; Sokolova, Y. Microsporidia–emergent pathogens in the global food chain. Trends Parasitol. 2016, 32, 336–348.
  89. Vávra, J.; Horák, A.; Modrý, D.; Lukeš, J.; Koudela, B. Trachipleistophora extenrec n. sp. a new microsporidian (Fungi: Microsporidia) infecting mammals. J. Eukaryot. Microbiol. 2006, 53, 464–476.
  90. Vávra, J.; Kamler, M.; Modrý, D.; Koudela, B. Opportunistic nature of the mammalian microsporidia: Experimental transmission of Trachipleistophora extenrec (Fungi: Microsporidia) between mammalian and insect hosts. Parasitol. Res. 2011, 108, 1565–1573.
  91. Schrögel, P.; Wätjen, W. Insects for food and feed-safety aspects related to mycotoxins and metals. Foods 2019, 8, 288.
  92. Evans, N.M.; Shao, S. Mycotoxin Metabolism by Edible Insects. Toxins 2022, 14, 217.
  93. Gałęcki, R.; Sokół, R. A parasitological evaluation of edible insects and their role in the transmission of parasitic diseases to humans and animals. PLoS ONE 2019, 14, e0219303.
  94. Yamada, M.; Tegoshi, T.; Abe, N.; Urabe, M. Two Human Cases Infected by the Horsehair Worm, Parachordodes sp.(Nematomorpha: Chordodidae), in Japan. Korean J. Parasitol. 2012, 50, 263.
  95. Jorjani, O.; Bahlkeh, A.; Koohsar, F.; Talebi, B.; Bagheri, A. Chronic respiratory allergy caused by Lophomonas blattarum: A case report. Med. Lab. J. 2018, 12, 44–46.
  96. Pappas, P.W.; Barley, A.J. Beetle-to-beetle transmission and dispersal of Hymenolepis diminuta (Cestoda) eggs via the feces of Tenebrio molitor. J. Parasitol. 1999, 85, 384–385.
  97. Manga-González, M.Y.; González-Lanza, C.; Cabanas, E.; Campo, R. Contributions to and review of dicrocoeliosis, with special reference to the intermediate hosts of Dicrocoelium dendriticum. Parasitology 2001, 123, 91–114.
  98. Bailey, W.; Cabrera, D.; Diamond, D. Beetles of the family Scarabaeidae as intermediate hosts for Spirocerca lupi. J. Parasitol. 1963, 49, 485–488.
  99. Thyssen, P.J.; Moretti, T.d.C.; Ueta, M.T.; Ribeiro, O.B. The role of insects (Blattodea, Diptera, and Hymenoptera) as possible mechanical vectors of helminths in the domiciliary and peridomiciliary environment. Cad. De Saúde Pública 2004, 20, 1096–1102.
  100. Graczyk, T.K.; Cranfield, M.R.; Fayer, R.; Bixler, H. House flies (Musca domestica) as transport hosts of Cryptosporidium parvum. Am. J. Trop. Med. Hyg. 1999, 61, 500–504.
  101. Goodwin, M.A.; Waltman, W.D. Transmission of Eimeria, viruses, and bacteria to chicks: Darkling beetles (Alphitobius diaperinus) as vectors of pathogens. J. Appl. Poult. Res. 1996, 5, 51–55.
  102. Aelami, M.H.; Khoei, A.; Ghorbani, H.; Seilanian-Toosi, F.; Poustchi, E.; Hosseini-Farash, B.R.; Moghaddas, E. Urinary canthariasis due to Tenebrio molitor Larva in a ten-year-old boy. J. Arthropod-Borne Dis. 2019, 13, 416.
  103. Gałęcki, R.; Michalski, M.M.; Wierzchosławski, K.; Bakuła, T. Gastric canthariasis caused by invasion of mealworm beetle larvae in weaned pigs in large-scale farming. BMC Vet. Res. 2020, 16, 1–7.
  104. Nguyen, N.; Yang, B.-K.; Lee, J.-S.; Yoon, J.U.; Hong, K.-J. Infestation status of the darkling beetle (Alphitobius diaperinus) in Broiler chicken houses of Korea. Korean J. Appl. Entomol. 2019, 58, 189–196.
  105. Maciel-Vergara, G.; Jensen, A.; Lecocq, A.; Eilenberg, J. Diseases in edible insect rearing systems. J. Insects Food Feed. 2021, 7, 621–638.
  106. Gahukar, R.T. Edible insects collected from forests for family livelihood and wellness of rural communities: A review. Glob. Food Secur. 2020, 25, 100348.
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Remigiusz Gałęcki
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